Mass Extinctions and Clade Extinctions in the History of Brachiopods: Brief Review and a Post-Paleozoic Case Study

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Rivista Italiana di Paleontologia e Stratigrafia (Research in Paleontology and Stratigraphy) vol. 125(3): 711-724. November 2019

MASS EXTINCTIONS AND CLADE EXTINCTIONS IN THE HISTORY OF BRACHIOPODS: BRIEF REVIEW AND A POST-PALEOZOIC CASE STUDY

ATTILA VÖRÖS1,2*, ÁDÁM T. KOCSIS2,3 & JÓZSEF PÁLFY2,4

1*Corresponding author. Department of Paleontology and Geology, Hungarian Natural History Museum, POB 137, Budapest H-1431, Hungary. E-mail: [email protected] 2MTA-MTM-ELTE Research Group for Paleontology, POB 137, Budapest H-1431, Hungary. 3GeoZentrum Nordbayern, Department of Geography and Geosciences, University of Erlangen-Nuremberg, Loewenichstraße 28, 91054 Erlangen, Germany. E-mail: [email protected] 4Department of Geology, Eötvös University, Pázmány Péter sétány 1/C, Budapest H-1117, Hungary. E-mail: [email protected]

To cite this article: Vörös A., Kocsis Á.T. & Pálfy J. (2019) - Mass extinctions and clade extinctions in the history of brachiopods: brief review and a post-Paleozoic case study. Riv. It. Paleont. Strat., 125(3): 711-724.

Keywords: Rhynchonelliformea; diversity; spire-bearers; biotic crises; end-Triassic; Toarcian.

Abstract. Brachiopods are a key group in Phanerozoic marine diversity analyses for their excellent fossil record and distinctive evolutionary history. A genus-level survey of raw diversity trajectories allows the identification of the Brachiopod Big Five, episodes of major genus losses in the phylum which are compared with the established Big Five mass extinctions of Phanerozoic marine invertebrates. The two lists differ in that the end-Cretaceous extinction appears subdued for brachiopods, whereas the mid-Carboniferous is recognized as an event with significant loss of brachiopod genera. At a higher taxonomic level, a review of temporal ranges of rhynchonelliform orders reveals episodes of synchronous termination of multiple orders, here termed clade extinctions. The end-Ordovician, Late Devonian and end-Permian events are registered as both mass extinctions and clade extinctions. The Late Cambrian and the Early Jurassic are identified as the other two clade extinction events. Coincident with the Early Toarcian oceanic anoxic event, the last clade extinction of brachiopods is defined by the disappearance of the last two spire- bearing orders, Athyridida and Spiriferinida. Their diversity trajectory through the recovery after the end-Permian crisis parallels that of the extant terebratulides and rhynchonellides until a Late Triassic peak but diverge afterwards. The end-Triassic diversity decline and Toarcian vanishing of spire-bearers correspond with contraction in their spatial distribution. The observed patterns and extinction selectivity may be explained both ecologically and physiologically. The specialized adaptation of morphologically diverse spire-bearers, as well as their fixed lophophore and passive feeding put them at a disadvantage at times of environmental crises, manifest in their end-Triassic near-extinction and Toarcian demise. Similar analyses of other clade extinctions may further improve our understanding of drivers and processes of extinction.

Introduction and became a subordinate player in the shallow-marine benthic communities after the end-Permian bi- Brachiopods are a key fossil group in the otic catastrophe. Paleozoic evolutionary fauna of Sepkoski (1981), During their Paleozoic heyday, brachiopods characterized by a distinctive diversity history. The developed free-lying, semi-infaunal and possibly phylum reached the peak of its adaptive and evolu- free-swimming ways of life and extremely varied tionary success in the second half of the Paleozoic morphologies and ornamentation styles, and at- tained extremely high taxonomic diversity (Rud- Received: February 28, 2019; accepted: August 1, 2019 wick 1970; Curry & Brunton 2007). (Note that in 712 Vörös A., Kocsis Á.T. & Pálfy J.

Mass extinctions and clade extinctions in the history of brachiopods

The following brief review will focus on the history of the subphylum Rhynchonelliformea (Articulata auctt.) which chiefly accounts for the dramatic changes in brachiopod diversity, much more than the other two subphyla, the Linguli- formea and Craniiformea. Changes in the generic abundance of brachiopods (Curry & Brunton 2007) clearly show the signs of several crises in ancient marine ecosystems. Most of the Big Five Fig. 1 - Number of brachiopod genera during the Phanerozoic (af- mass extinctions appear also on this brachiopod ter Curry & Brunton 2007) and the number of genera that became extinct at the Brachiopod Big Five (indicated by ar- diversity curve: the end-Ordovician, Late Devoni- rows). an, end-Permian and end-Triassic events are eas- ily recognizable (Fig. 1). On the other hand, the this study, we use the term diversity to refer to sim- famous fifth of the Big Five, the end-Cretaceous ple taxic richness, either at species, genus or higher event, appears subdued and was perhaps less dra- taxonomic level). However, after the end-Permian matic for brachiopods. Alternatively, a more rapid crisis and during the Mesozoic marine revolution recovery may have masked the diversity decrease at (Vermeij 1977), rhynchonelliform brachiopods re- low temporal resolution (Alroy et al. 2008). Of the turned to the conservative modes of life with pedi- four events of the Brachiopod Big Five that clearly cle attachment or cementation and, as reflected by coincide with the classical Big Five, the greatest was their considerably reduced diversity, were outcom- the end-Permian with 308 genera becoming extinct, peted by bivalves (Gould & Calloway 1980; Thayer closely followed by the Late Devonian (256). The 1985; Walsh 1996). end-Ordovician event ranks third (108), whereas The long and eventful history of the phylum the end-Triassic appears the smallest of the brachi- Brachiopoda is replete with extinction events of opod mass extinctions with the disappearance of different magnitudes. The major drops in the clas- 72 genera (data from Curry & Brunton 2007). Con- sical diversity curve of marine invertebrates (Raup versely, the fourth in rank among the Brachiopod & Sepkoski 1982), i.e. the originally identified “Big Big Five, in the mid-Carboniferous with 84 genera Five” mass extinctions, are unquestionably recog- becoming extinct, does not correspond to any of nizable in the updated generic abundance curve of the classical Big Five. brachiopods (Curry & Brunton 2007). However, Mass extinctions are commonly analyzed at there are some important differences in the magni- low taxonomic levels and measured in terms of ra- tude, timing, and significance of these events. Some tio of taxic loss across stratigraphic boundaries. For of these deviations are discussed in this paper. our study, the Brachiopod Big Five extinctions and In the first part, we briefly review the dif- the post-Paleozoic decline are demonstrated using ferences between the established Big Five and the the simple count of genera. On the other hand, “Brachiopod Big Five” events, i.e. the five greatest it seems also worthwhile to analyze the extinction mass extinctions of brachiopods, in terms of ge- events and the decline of the phylum at a high- neric abundance. We also introduce here the term er taxonomic level. In the case of Rhynchonelli- “clade extinction”, a useful concept to discuss ex- formea (Articulata) the highest meaningful level is tinctions at the higher taxonomic level of orders, the rank of orders. The extinction events that mark for those events when entire brachiopod clades van- the final disappearances of orders are termed here ished. The second part presents a case study with a clade extinctions, because these events involve ul- concise discussion of the last, post-Paleozoic clade timate, definitive losses of the brachiopod groups extinction of the brachiopods in the Early Jurassic. concerned. Mass extinctions and clade extinctions in the history of brachiopods 713

Fig. 2 - Comparison between the major mass extinctions (the Brachiopod Big Five) and the clade extinctions (extinctions of orders) among brachiopods. Range charts after Carlson (2007).

The range chart of the orders of Rhyn- Brachiopod Big Five. Admittedly, such compila- chonelliformea, compiled by Carlson (2007) and tions may not fully capture the complexity of these adapted here (Fig. 2), shows that the changes in events, as the temporal resolution may be too crude number of orders principally follow the gener- to reveal the details, especially for the Paleozoic. ic diversity curve of Curry & Brunton (2007). It Nevertheless, the pattern of correspondence and starts with eight orders in the Cambrian, then, after divergence in diversity trajectories at low taxonom- the Devonian peak (12), decreases to nine in the ic levels and clade termination events is insightful. Permian, falls to five in the Triassic, and ends with In the Paleozoic history of the Rhynchonel- three extant orders. liformea, the mass and clade extinctions were com- More importantly, Figure 2 also shows that monly followed by rapid recoveries accompanied the clade extinctions, i.e. the ultimate disappear- by significant morphological innovations (Rudwick ances of orders, are not perfectly in agreement 1970; Curry & Brunton 2007). This pattern com- with the Brachiopod Big Five events. The end-Or- pletely changed after the end-Permian catastrophe. dovician, Late Devonian and, most remarkably, The four surviving orders, Rhynchonellida, Tere- the end-Permian extinctions are classified to both bratulida, Athyridida and Spiriferinida (joined by types of events. On the other hand, two very signif- Thecideida that emerged in the Triassic) show lim- icant clade extinctions occurred in the Late Cam- ited recovery and only minor diversity peaks in the brian (with four orders becoming extinct) and in Triassic and Jurassic, but largely without any sig- the Early Jurassic (with two orders lost), which do nificant morphological innovation. After the dev- not correspond to major losses on the generic di- astating end-Permian extinction, the last clade ex- versity curve, hence are not considered among the tinction in the history of brachiopods occurred in 714 Vörös A., Kocsis Á.T. & Pálfy J.

Fig. 3 - Temporal changes in the generic diversity (number of genera) of brachiopod groups in the Triassic and Early Jurassic. A) Diversity of the spire-bearer orders (Athyridida and Spiriferinida) and the other orders; B) diversity of the orders Athyridida, Spiriferinida, Rhyn- chonellida and Terebratulida.

the Early Jurassic, in the Early Toarcian, when the Material and methods orders Athyridida and Spiriferinida vanished. Albe- it commonly considered only a second-order ex- Genus-level occurrence data for the Triassic to Early Jurassic tinction event, this minor biotic crisis has received distribution of Athyridida, Spiriferinida, Rhynchonellida and Tere- bratulida were collected from the respective volumes of the Treatise considerable attention (Little 1996; García Joral et on Invertebrate Paleontology (Álvarez & Rong 2002; Savage et al. al. 2011, 2018; Caruthers et al. 2013; Danise et al. 2002; Carter & Johnson 2006; Lee et al. 2006, 2007; Gourvennec & 2018; Piazza et al. 2019) for its coincidence with the Carter 2007; Curry & Brunton 2007). The Early Jurassic part was Early Toarcian oceanic anoxic event also known as further resolved from the level of stages to the level of substages, to better constrain the diversity trajectories in the critical, terminal part Jenkyns Event (Müller et al. 2017). Herein we ex- of the spire-bearers’ evolutionary history. plore its significance for brachiopods as the last Further data for the stratigraphic distribution and range- clade extinction in this phylum. The peculiarity of through diversities of the spire-bearing brachiopods (Athyridida, Spiriferinida) at species-level were collected manually from the avail- this event lies in the fact that the last two orders of able literature, thereby extending the coverage by data not meeting previously successful and anatomically distinctive the entry criteria of PaleoDB (Diener 1920; Alméras 1964; Dagys spire-bearing forms were lost. 1974; Siblík 1983, 1988, 2001; Vörös 2002; Comas-Rengifo et al. 2006; Vörös & Dulai 2007). Diversity curves at the genus and species level were constructed for the Triassic to Early Jurassic interval, calibrated with the time scales of Mundil et al. (2010) and Gradstein Analysis of the last clade extinction et al. (2012). of brachiopods To track the spatial distribution changes of spire-bearers, Paleobiology Database (PaleoDB) occurrence data of brachiopods In this case study we present an analysis of from the Triassic to Jurassic interval were downloaded on 17.01.2019. and were resolved to the stratigraphic level of stages. The paleocoor- the extinction process of the two spire-bearer or- dinates of the collections were rotated to match the paleogeograph- ders surviving the end-Permian, Athyridida and ic reconstructions of the PALEOMAP PaleoAtlas project (Scotese, Spiriferinida, i.e. the victims of the last clade ex- 2016). The prepared dataset consists of 8,429 occurrences from 3,680 collections in the Late Triassic-Early Jurassic interval. tinction event in the history of brachiopods. The The spire-bearer genera were grouped into four morphotype study is focused on four rhynchonelliform orders: categories: biconvex (i.e. short-hinged, globose), concavo-convex Rhynchonellida, Athyridida, Spiriferinida and Te- (leptaenoid), expanded (alate), and inaequivalve, conical (cyrtini- rebratulida. The fifth post-Paleozoic order, Theci- form). The occurrences of the genera attributed to these morphotypes were counted by ages of the Triassic to Early Jurassic interval deida is considered of minor significance and not based on the Treatise on Invertebrate Paleontology (Álvarez & Rong included in our analysis. 2002; Carter & Johnson 2006; Gourvennec & Carter 2007). Mass extinctions and clade extinctions in the history of brachiopods 715

Fig. 4 - Temporal changes in the taxic diversity (i.e. richness) of the spire-bearer orders (Athyridida and Spiriferinida) in the Triassic and Early Jurassic. A) Number of genera; B) number of species.

Results ary bloom in the Early Jurassic (Fig. 4B). The Pliens- bachian peak of Spiriferinida is especially notewor- The generic diversity of the spire-bearer and thy, almost reaching their Triassic maximum value. the other, non-spire-bearer clades that survived the The geographical occurrence patterns of the end-Permian show similar trajectories in the Triassic two spire-bearer orders (Athyridida, Spiriferinida) then, after an end-Triassic bottleneck, their trends and the other (non-spire-bearer) brachiopod orders markedly deviate in the Jurassic (Fig, 3A). The four (Rhynchonellida and Terebratulida) are presented in brachiopod orders analyzed initially follow a simi- successive maps from the Norian to the Toarcian lar trajectory: their Triassic recovery reached a max- (Figs. 5, 6). The geographic range of spire-bearing imum in the Carnian and Norian. However, the brachiopods considerably decreased after the Trias- end-Triassic bottleneck of the Rhynchonellida and sic-Jurassic boundary, compared to other forms. Terebratulida was followed by a secondary bloom in The changes in proportion of morphologi- the Early Jurassic, whereas the end-Triassic near-ex- cal types of spire-bearing genera during the Trias- tinction of the spire-bearer Athyridida and Spirife- sic-Jurassic interval are summarized in Tables 1 and rinida was succeeded by only a subdued diversity 2. In the Triassic, different adaptive morphotypes increase in the Early Jurassic and vanishing in the were abundant in both spire-bearing orders. After Toarcian (Fig. 3B). the end-Triassic extinction, the alate and cyrtiniform The species diversity curves for the spire-bear- morphotypes, besides the conservative biconvex er orders differ considerably from the trajectories of shells, persisted up to the Early Toarcian among the their generic diversity (Fig. 4A, B). The number of Spiriferinida. The order Athyridida was represent- spiriferinid genera continuously exceeds that of the ed exclusively by the leptaenoid morphotype in the athyridides, especially in the Triassic. On the other Early Jurassic. hand, the species diversity of the athyridides significantly surpasses that of the spiriferinids at the Triassic (Carnian) maximum (Fig. 4B). The Early Ju- Discussion rassic parts of the generic diversity curves display persistently low values for both spire-bearer orders. Demise of the last two spire-bearing brachiopod or- In contrast, their species diversities show a second- ders. Statistical analyses of diversity histories and tax- Vörös A., Kocsis Á.T. & Pálfy J. 716Table 1 Attribution of athyridid genera to different morphotypes and their distribution in the Triassic to Early Jurassic interval

Tab. 1 - Attribution of athyridid genera to different morpho-

types and their distribution

Morphotype Genus in the Triassic to Early Juras-

sic interval. Early Triassic Early Anisian Ladinian Carnian Norian Rhaetian Hettangian Sinemurian Pliensbachian Toarcian Amphitomella x Anisactinella x x x Anomactinella x x Dioristella x Diplospirella x Euractinella x x Hustedtiella x Majkopella x x x Misolia x Neoretzia x x x x biconvex Ochotathyris x Oxycolpella x x x Pentactinella x x Pexidella x x x x Qingthyris x x Schwagerispira x x x Septospirigerella x x x x x x Spirigerellina x x x x Stolzenburgiella x x Tetractinella x x total biconvex 3 9 12 14 7 3 Amphiclina x x x Amphiclinodonta x x x x x x Carinokoninckina x x x Koninckella x x x x x x x leptaenoid Koninckina x x x Koninckodonta x x x Lamellokoninckina x x x Septamphiclina x x x total leptaenoid 7 7 7 2 3 3 2 alate Clavigera x x total alate 1 1 Cassianospira x cyrtiniform Hungarispira x total cyrtiniform 2 onomic rates of spire-bearing vs. non-spire-bearing articulate brachiopod orders diverged significantly. brachiopods confirm that the spire-bearing groups The end-Triassic extinction appeared as a signif- were indeed significantly more affected by both the icant bottleneck for all of them, while the Early end-Triassic and Early Toarcian environmental cri- Toarcian event, a minor bottleneck for the rhyn- ses (Figs. 3, 4). Both spire-bearing orders reached chonellides and terebratulides, was a clade extinc- their maximum Triassic diversity in the Carnian tion for the spire-bearer Athyridida and Spirifer- and were only slightly surpassed by terebratulides inida. and rhynchonellides in the Norian. Athyridida and The end-Triassic bottleneck and the Early Toarcian Spiriferinida were severely affected by the end-Tri- extinction in time and space. Both the end-Triassic assic crisis and had a short and limited recovery bottleneck in the diversity and the Toarcian partial before their final extinction in the Early Toarcian extinction are reflected in the spatial distribution Jenkyns Event, providing an example of the “dead of brachiopods (Figs. 5, 6). In the Late Triassic, clade walking” concept of Jablonski (2001; 2002). all of the four rhynchonelliform orders were glob- The demise of the Athyridida and Spiriferinida was ally distributed. By the Hettangian, the scatter of the last clade extinction, registering the loss of two their occurrences became strongly reduced, with a orders within the phylum Brachiopoda. focus in the western Tethys (including the Gond- The worldwide end-Triassic and Toarcian wanan and Laurasian seaways), and a similar spatial extinction events imposed severe contractions in contraction is seen in the Toarcian. the taxonomic diversity of brachiopods. Howev- The geographical distribution of the two er, the post-Permian diversity history of the four spire-bearing orders even more clearly demon- Mass extinctions and clade extinctions in the history of brachiopods 717

Tab. 2 - Attribution of spiriferinid

genera to different morpho-

types and their distribution

Morphotype Genus Triassic in the Triassic to Early Juras- sic interval. Early Anisian Ladinian Carnian Norian Rhaetian Hettangian Sinemurian Pliensbachian Toarcian

Aequspiriferina x x x x x Altoplicatella x x Balatonospira x Calyptoria x x x x Canadospira x Dagyspirifer x Dentospiriferina x Dinarispira x x Hirsutella x x Jiangdaspirifer x x x Koeveskallina x x x Laballa x x x Liospiriferina x x x x Madoia x x Mentzelia x x x x x Mentzelioides x x x Mentzeliopsis x Orientospira x biconvex Paramentzelia x x x Pennospiriferina x x x x Pseudolaballa x Pseudospondylospira x x Psioidea x Qinghaispiriferina x x Qispiriferina x x Sinucosta x x x x x Sinucostella x x Spiriferina x x x Spiriferinoides x Spondylospiriferina x x Tethyspira x Triadispira x x Tylospiriferina x x x Viligella x Yalongia x x total biconvex 12 16 18 14 10 3 3 3 2 Alipunctifera x Boreiospina x x Callospiriferina x x x Dispiriferina x x x Lancangjiangia x x x Nudispiriferina x x Pseudospiriferina x x alate Psioidella x x x Punctospirella x x Qingyenia x x Rastelligera x x Tulungospirifer x Yangkongia x x Yanospira x total alate 6 7 4 4 2 2 2 2 Bittnerula x Bolilaspirifer x x x Cisnerospira x x x Flabellocyrtia x Klipsteinella x Klipsteinelloidea x x x Leiolepismatina x x Lepismatina x x x x x Neocyrtina x x Paralaballa x x x cyrtiniform Paralepismatina x Phenacozugmayerella x x Pseudocyrtina x Pseudolepismatina x x x x x x Spinolepismatina x x x Spondylospira x x Suessia x x x x Thecocyrtella x x x Thecocyrtelloidea x Vitimetula x Zugmayerella x x total cyrtiniform 1 6 5 11 12 8 1 2 2 2 718 Vörös A., Kocsis Á.T. & Pálfy J.

Fig. 5 - Geographic occurrence pat- 90 ● ● terns of brachiopods in the ● ●● Norian A), Rhaetian B) and ● ●●

60 ● Hettangian C), based on ● ●●●

● the data deposited in the ● ●● ● ● ● ●●● ● PaleoDB. Polygons indicate 30 ●● ● ●● ● ● ● ● ● ●● ●●● convex hulls of occurrence ● ● ● ● ●● in the projection. The geo- 0 ● ● graphic range of Spiriferini- ● ● ● ● da is indicated by orange dots ●

−30 and gold colored shadow; Athyridida that of the Athyridida by red ● ● Spiriferinida triangles and cross-hatching; −60 other ●● rhynchonellid and terebratu- A lid occurrences marked by

−90 green open diamonds. Pale- −180 −150 −120 −90 −60 −30 0 30 60 90 120 150 180 ogeographic reconstructions 90 ● are from the PALEOMAP

● PaleoAtlas project (Scotese ● ●● 2016). 60 ● ●

●●●●●● ● ● ●

30 ●● 0

●

● −30 ●

●

● ● −60 ●● B −90 −180 −150 −120 −90 −60 −30 0 30 60 90 120 150 180 90 60

● ●●●● ● 30 0 −30 −60 C −90 −180 −150 −120 −90 −60 −30 0 30 60 90 120 150 180 strates this spatial bottleneck. Their worldwide Late cluding the Madagascar seaway of the Gondwanan Triassic distribution shrank to the western part of epicontinental sea (Baeza-Carratalá et al. 2018), the Tethys in the Hettangian (Fig. 5C). The athyri- with the exception of a single occurrence in New dids (represented solely by the leptaenoid koninc- Zealand (Damborenea & Manceñido 1992) (Fig. kinids) remained restricted to the western end of 6C). On the other hand, the non-spire-bearing or- the Tethys with a limited expansion to the Laur- ders Rhynchonellida and Terebratulida regain their asian Seaway [Bjerrum et al. (2001), also known worldwide distribution in the Pliensbachian (Fig. as the Viking Corridor (Westermann 1993)], just 6B), a pattern seen in the rest of the Jurassic. The prior to their extinction in the Early Toarcian (Fig. almost complete withdrawal of the “dead clades” 6C). The spiriferinids re-appear in the eastern Pan- to the western parts of the Tethys seems to sup- thalassa in the Sinemurian and Pliensbachian (Fig. port the idea that this part of the Mesozoic ocean 6B), but their last, Toarcian occurrences seem con- was the most important refuge, a “lost Eden” for fined again to the western parts of the Tethys, in- brachiopods (Vörös 1993, 2005). Mass extinctions and clade extinctions in the history of brachiopods 719

Fig. 6 - Geographic occurrence patterns of brachiopods in the 90 Sinemurian A), Pliensbachi-

an B) and Toarcian C), based 60 ● ● on the data deposited in the ●● ●● ● ● ● ● ● ● ●● PaleoDB. Polygons indicate 30 ● ● ● convex hulls of occurrence ●

in the projection. The geo- 0 graphic range of Spiriferini- da is indicated by orange dots ●

and gold colored shadow; −30 that of the Athyridida by red triangles and cross-hatching; rhynchonellid and terebrat- −60 ulid occurrences marked by A −90 green open diamonds. Pale- −180 −150 −120 −90 −60 −30 0 30 60 90 120 150 180 ogeographic reconstructions

are from the PALEOMAP 90 PaleoAtlas project (Scotese 2016). ● 60 ●

● ● ● ● ● ●● ●●●● ●● ● ● ● 30 ● ● ●●● 0

● ● ● −30

−60 B −90 −180 −150 −120 −90 −60 −30 0 30 60 90 120 150 180 90 60

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● −30 −60 ● C −90 −180 −150 −120 −90 −60 −30 0 30 60 90 120 150 180

Drivers of the selective extinction of spire-bearers. In the Triassic to Jurassic spire-bearing clades and search of possible controls on the observed pattern their inferred environmental and substrate prefer- of selective extinction, our first assumption consid- ences are shown in Figure 7. The environmental in- ers the differences between adaptive strategies de- terpretations are based mainly on previous studies veloped by the spire-bearer clades and by the other by Ager (1968), Rudwick (1970), Vörös (2002) and brachiopod groups. Morphological adaptation to Baeza-Carratalá et al. (2016). various environments and substrates was manifold The changes in the proportion of morpho- and contributed to the evolutionary success of bra- logical types of spire-bearing genera during the chiopods in the Paleozoic. During their secondary Triassic to Early Jurassic interval are illustrated diversity increase in the Triassic, the athyridides and in Figure 8. In the Triassic, besides the biconvex spiriferinides repeatedly evolved various adaptive shells, different adaptive morphotypes were wide- morphologies, besides the conservative biconvex spread in both spire-bearing orders. For the spirif- shell form. The basic morphological types among erinides, the pattern remained the same in the Early 720 Vörös A., Kocsis Á.T. & Pálfy J.

The second assumption about possible controls on selective extinction considers the differences of the feeding mechanism and efficiency between the spire-bearing and other brachiopods. Here we suggest that the selective extinction of the spire-bearing clades is best explained by their internal features: the spiral brachidium and the lophophore firmly attached to it. The disadvantages of the spirolophe re- Fig. 7 - Main morphological types among the spire-bearing clades and their inferred environmental and substrate preferenc- strained by calcareous spiralia were first emphasized es (after Ager 1967; Rudwick 1970; Vörös 2002 and Bae- by Ager (1987) who explained the Toarcian extinc- za-Carratalá et al. 2016). tion of spiriferinides by this drawback. He also stressed that the unbound and flexible lophophore Jurassic, whereas the morphological disparity of the of the rhynchonellides, though also of spirolophe athyridides was largely confined to the Triassic: their type, was an advantage in the adverse environments Early Jurassic representatives, the koninckinides all during the anoxic event and facilitated the survival belong to the leptaenoid morphotype. Apparently, of the order Rhynchonellida. athyridides lost the adaptive flexibility, what may be Many authors attempted to reconstruct the considered as a herald of incoming extinction of filter-feeding mechanism of the extinct brachiopods this clade. However, not only the Athyridida but the with spiral brachidia (e.g. Rudwick 1970; Vogel 1975). other spire-bearing clade was also eradicated at the Recently Manceñido & Gourvennec (2008) reviewed Early Toarcian Jenkyns Event. the previous research and ideas on the feeding cur- The various (alate, cyrtiniform and leptaenoid) rent system of spire-bearing brachiopods. They con- morphotypes were strongly dependent on environ- cluded that the alate spire-bearers used their laterally ment (substrate, currents and food supply). Adap- oriented spiralia and spirolophs as a plankton mesh tation by itself involves environmental dependence, involving a passive flow system with a median inhal- which may become detrimental in hard times of ant and two lateral exhalant sectors. This circulation environmental stress, leading to biotic crisis. The pattern is opposite to the feeding current systems of most important competitors of the semi-infaunal the recent articulate brachiopods, where the outflow and soft-bottom dweller morphotypes were certain- jet is always medially located (Rudwick 1970; Vogel ly the bivalves. By their biological advantages, they 1975). The model by Manceñido & Gourvennec displaced the brachiopods from most of the shallow (2008) was convincingly supported using flume ex- marine environments. This pre-emptive exclusion periments by Shiino et al. (2009) and Shiino (2010). was repeated after each mass extinction, notably The latter authors constructed transparent models after the end-Permian and the end-Triassic (Walsh of Devonian spiriferides both with alate and reg- 1996) and increased during the Mesozoic marine ular, biconvex form. The flow tests demonstrated revolution (Vermeij 1977; 2008). This competi- that the continuous stream of the surrounding wa- tion primarily affected the more specialized, highly ter generated a medial inflow current into the gaping adapted morphotypes of spire-bearing brachiopods shell models and wide zones of outflows along the and might be a decisive factor in their end-Triassic lateral sides. Besides, they revealed the presence of a decline and final demise in the Early Toarcian. On constant spiral flow system inside the valves closely the other hand, the less specialized morphology, the following the laterally oriented spiral brachidium of active pedicle and the broader environmental toler- the model specimens. ance allowed rhynchonellides and terebratulides to It may be concluded that the extinct spirif- survive crises in refugia, e.g. in submarine crevices erides were adapted to steady, low-velocity currents and cavities. As a result, the conservative, epifaunal of the bottom water, where the passive gyrate flows biconvex shells of Rhynchonellida and Terebratulida carried the suspended food particles directly to the proved to be successful during the extinction events tentacles of the lophophore. This is a passive feed- and enabled the survival and recovery of these ex- ing mechanism in contrast to the active pump sys- tant groups. tem of other articulate brachiopods. In present-day Mass extinctions and clade extinctions in the history of brachiopods 721

Fig. 8 - Temporal changes in the proportion of morphological types of spire-bearing genera during the Triassic to Early Jurassic interval. A) Spiriferinida, B) Athyridida.

rhynchonellides and terebratulides the activity of ments. The physiological advantage of these orders cilia aligned on the lophophore generates inflows helped them to cope better during the critical envi- through the lateral gape and jet-like anterior out- ronmental changes at the end of the Triassic and flows, and they maintain this system even in the ab- in the Early Toarcian, when the spire-bearing clades sence of bottom currents (Rudwick 1970; Peck et were more severely affected and ultimately became al. 1997). extinct. The passive feeding system of the spire-bearing brachiopods was advantageous in stable, cur- Conclusions rent-dominated, shallow marine habitats, as it is proved by their Paleozoic fossil record (Álvarez A comparison of the history of genus-level 2006). However, the expense of the success was raw taxonomic diversity in the phylum Brachiopo- an environmental dependence which proved to be da with the overall Phanerozoic pattern of marine detrimental during the unfavorable environmental invertebrate diversity reveals that four of the estab- conditions in times of biotic crises and resulted in lished Big Five mass extinctions also rank among partial or total extinctions. On the other hand, the the Brachiopod Big Five extinction events. Only the active feeding of terebratulides and rhynchonellides end-Cretaceous extinction appears less significant was effective in deeper or calmer seawaters. Their for brachiopods and is surpassed in terms of taxic broader depth range may have helped survival of loss by the mid-Carboniferous. Further insights can anoxic events by affording colonization of habitats be gained from diversity analyses at higher taxonom- outside of temporarily oxygen-depleted environ- ic levels. The synchronous loss of two or more bra- 722 Vörös A., Kocsis Á.T. & Pálfy J.

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